Sunday, July 26, 2015

The following has been adapted from a press release and a blog post, with some light editing by me (JCM).

A new fossil, named Tetrapodophis amplectus, claims to be a four-legged, burrowing
snake. (A) Counterpart, showing skull and skeleton impression. (B) Main slab,
showing skeleton and skull impression. Figure 1 from Martill et al. 2015. (C) The snake has small ‘hands’ that are
approximately 1cm long. Credit: Image courtesy of University of Portsmouth.

The first known
fossil of a four-legged snake, and the team -- led by Dr. Dave Martill from the
University of Portsmouth -- say that this discovery could help scientists to
understand how snakes lost their legs. The research was published in the
journal Science.

Dr Martill said:
"It is generally accepted that snakes evolved from lizards at some point
in the distant past. What scientists don't know yet is when they evolved, why
they evolved, and what type of lizard they evolved from. This fossil answers
some very important questions, for example it now seems clear to us that snakes
evolved from burrowing lizards, not from marine lizards."

The fossil, from
Brazil, dates from the Cretaceous period and is 110 million years old, making
it the oldest definitive snake. Martill discovered the fossil as part of a
routine field trip with students to Museum Solnhofen, Germany, a museum that is
well-known for its prestige with regard to fossils.

Dr Martill said:
"The fossil was part of a larger exhibition of fossils from the Cretaceous
period. It was clear that no-one had appreciated its importance, but when I saw
it I knew it was an incredibly significant specimen."

Martill worked
with expert German palaeontologist Helmut Tischlinger, who prepared and
photographed the specimen, and Nick Longrich from the University of Bath's
Milner Centre for Evolution, who studied the evolutionary relationships of the
snake.

Dr Longrich, who
had previously worked on snake origins, became intrigued when Martill told him
the story over a pint at the local pub in Bath.

He said: "A
four-legged snake seemed fantastic and as an evolutionary biologist, just too
good to be true, it was especially interesting that it was put on display in a
museum where anyone could see it."

He said he was
initially skeptical, but when Dr Martill showed him Tischlinger's photographs,
he knew immediately that it was a fossil snake.

The snake, named Tetrapodophis amplectus by the team, is
a juvenile and very small, measuring just 20 cm from head to toe, although it may
have grown much larger. The head is the size of an adult fingernail, and the
smallest tail bone is only a quarter of a millimeter long. But the most
remarkable thing about it is the presence of two sets of legs, or a pair of
hands and a pair of feet.

The front legs are
very small, about 1cm long, but have little elbows and wrists and hands that
are just 5mm in length. The back legs are slightly longer and the feet are
larger than the hands and could have been used to grasp its prey.

Dr Longrich said:
"It is a perfect little snake, except it has these little arms and legs,
and they have these strange long fingers and toes.

"The hands
and feet are very specialized for grasping. So when snakes stopped walking and
started slithering, the legs didn't just become useless little vestiges -- they
started using them for something else. We're not entirely sure what that would
be, but they may have been used for grasping prey, or perhaps mates."

Interestingly, the
fossilized snake also has the remains of its last meal in its guts, including
some fragments of bone. The prey was probably a salamander, showing that snakes
were carnivorous much earlier in evolutionary history than previously believed.

Helmut Tischlinger
said: "The preservation of the little snake is absolutely exquisite. The
skeleton is fully articulated. Details of the bones are clearly visible and
impressions of soft tissues such as scales and the trachea are preserved."

Tetraphodophis has been categorized as a snake, rather
than a lizard, by the team due to a number of features:

· The skeleton has
a lengthened body, not a long tail.

· The tooth
implantation, the direction of the teeth, and the pattern of the teeth and the
bones of the lower jaw are all snake-like.

· The fossil
displays hints of a single row of belly scales, a sure fire way to
differentiate a snake from a lizard.

Tetrapodophis would have lived on the bank of a salt
lake, in an arid scrub environment, surrounded by succulent plants. It would
probably have lived on a diet of small amphibians and lizards, trying to avoid
the dinosaurs and pterosaurs that lived there.

At the time, South
America was united with Africa as part of a supercontinent known as Gondwana.
The presence of the oldest definitive snake fossil in Gondwana suggests that
snakes may originally have evolved on the ancient supercontinent, and only
became widespread much more recently.

However there is a
controversy brewing around the specimen, and it is not the creationist controversy
you might expect.

Discover Magazine’ blog has a piece
by Christie
Wilcox titled “Four-Legged Snake
Shakes Up Squamate Family Tree – Or Does It?” (posted July 24, 2015)

Ancestral state
analyses, use math and science to estimate the biological and ecological traits
of the most recent common ancestor of a group of species, suggested that early
snakes were nocturnal hunters, preying upon the small vertebrates of their era
through stealth, not constriction. Their analysis didn’t find that snakes were
burrowers, however — there was no strong support of a fossorial lifestyle, just
that the snakes lived on land.

According to
Hsiang, morphological data “strongly influenced” the snake tree. “Our study helped
to demonstrate how important and essential it is to include fossils when we are
trying to understand how and when organisms evolved.” In the paper, the author’s
note that the inclusion of fossil data resulted in relationships that would be
“unexpected” given current snakes, and that the fossils’ influence was
sustained “even when such data are vastly outnumbered by genetic sequence
data,” thus including the new fossil in a similar analysis might be even more
informative.

“Now that Martill et al.’s paper on Tetrapodophis has been published, the obvious next step is to
include it in large-scale, comprehensive analytical studies looking at snake
evolutionary history and phylogenies.”

Though there was
some excitement when Hsiang and her colleagues published their analysis in May,
a paper published a little over a month earlier in PLoS ONE slipped by the
press unnoticed. The analysis, led by Tod Reeder from San Diego State
University, looked beyond snakes to reconstruct the evolutionary relationships
within the squamates, the group of reptiles that contains lizards and snakes.
Using the largest dataset to date which, like Hsiang, included both genetic and
morphological markers, Reeder and his colleagues affirmed one of the crucial
pieces of evidence of a marine snake origin: the close relationship between
mosasaurs and snakes.

“The most
comprehensive analysis of the lizard evolutionary tree now reinstates these
aquatic mosasaurs as the nearest relatives to snakes,” explains Michael Lee, associate
professor at the University of Adelaide, who was one of the first scientists to
suggest that snakes may have started in the water.

The lizard tree,
which found the aquatic mosasaurs (Mosasauria) to be sister to modern snakes
(Serpentes).

The lizard
evolutionary tree, which places the aquatic mosasaurs (Mosasauria) sister to
modern snakes (Serpentes) rather than the group used by Hsiang et al. (Anguimorpha).

Because of this,
Reeder et al. calls into question the
methods used by Hsiang et al.,
specifically one of the core assumptions in the paper: the closest relatives of
snakes. When constructing evolutionary trees, assumptions have to be made to
“root” the tree, or put the relationships into the context with regards to
time. Scientists must compare their data to what is called an “outgroup”, which
is ideally the closest relative or relatives to the group of interest. Hsiang
and her colleagues used a subset of a group of lizards called anguimorphs,
which includes land dwelling lizards like varanids that includes the Komodo
dragon.

“The Hsiang paper
was a terrific analysis of the evolution within snakes, but the fundamental
core assumption they made in the paper was that terrestrial lizards were
ancestral to snakes,” said Lee. “The direction of evolution was determined by
that assumption. But if you assume, as the Reeder paper suggests, that
mosasaurs are ancestral to snakes, then some of the inferences by Hsiang might
not hold.”

Hsiang admits that
there are differences between the phylogenies in her paper and Reeder’s, and
that the choice of outgroup may have skewed their results. “There are
differences between the Reeder et al.
phylogeny and our phylogeny — it would be interesting to conduct an in-depth
analysis to try and determine why the differences in phylogeny exist,” she
said. While her team’s tree was strongly influenced by morphology, Reeder’s
team found that genetics most strongly predicted the results. “In fact, the
morphological data are really ambiguous,” co-author John Wiens said in a press
release. “Or in some cases, even worse than ambiguous.”

“There’s certainly
a possibility that our results would have been different if we had used
different outgroups, as phylogenetic and ancestral state reconstruction
analyses use the outgroup to determine the direction and polarity of character
state evolution,” said Hsiang. However, she doubts the impact would have been
large, as other close relatives of mosasaurs are land-lubbers. “Though the
inclusion of mosasaurs would likely have increased the probability of an
aquatic lifestyle for early snakes somewhat, this would probably have been
“balanced out” by the many anguimorph lizards that are not aquatic.”

“Of course, we’d
have to actually run the analysis to know for sure.”

Meanwhile, Bruno
Simões from the Natural History Museum, London, UK and his colleagues were
taking a very different approach to understanding snake evolution. Instead of
looking at bones and unrelated genes, they very specifically examined the genes
encoding for visual pigments in lizards and snakes. These genes are
well-studied, and in other groups like mammals, are correlated with behaviors
like burrowing and nocturnal activity.

“Visual pigments,
like opsin and rhodopsin, are basically the business front-ends of the visual
pathway,” says Simões. “So basically if anything is happening in the visual
system, the visual pigments will be the first to be impacted.” Burrowing
mammals, for example, have lost some visual pigment genes, as they no longer
need them underground. But even more impressively, scientists can connect
genetic changes in these pigment genes to ecology and function. “By checking
their amino acid composition, you can estimate what kind of wavelengths the
animal can see,” says Simões.

When Simões et al. compared the visual pigment genes
in snakes to other lizards, they found something exciting: snakes have lost two
of the five pigments found in the rest of the squamates. They retain the same
three that we have. Simões explained that this means snakes likely went through
an “ancestral nocturnal bottleneck,” just like mammals did. “Snakes have this
contrasting pattern from lizards that converges with mammals.”

Evolutionary tree
for the Rhodopsin 1 gene, the only one left in the most underground snakes.

Interestingly, in
fossorial lizards, all five pigments were still around, but in fossorial snakes
like the termite-decapitating blindsnakes, only one pigment remained. “The fact
that the visual system was not so reduced suggests that the ancestor for all
snakes was nocturnal, not fossorial” — a finding which coincides with the
ancestral state reconstructions found by Hsiang et al.

As for the question
of marine origins, Simões says that he “didn’t find evidence that it was a
marine animal.” Marine environments have very different light conditions than
terrestrial ones, with a quick loss of red wavelengths with depth, followed by
an eventual loss of all light in the deep sea. Marine animals eyes often show a
“shift in spectral tuning to a marine environment,” says Simões, which includes
a higher sensitivity for blue wavelengths. In sea snakes, for example, the
shorter-length opsin 1 becomes blue sensitive instead of UV sensitive. But
Simões found no such shift in all snakes.

“I think that it’s
a really interesting paper, in that they’ve discovered that snakes have lost a
whole bunch of visual genes that are found in other lizards, which does suggest
they went through some kind of semi-blind phase in their evolution,” says Lee.
But he still would like to see more research before discounting the aquatic
hypothesis. “One thing I’d like to see done is what genes are lost in living
marine reptiles like sea turtles,” said Lee, to see if there are any opsin
genes lost in other marine reptiles like the ones lost in snakes.

A Four-Legged
Snake?

Which brings us
back to the most recent finding, what Martill and his colleagues claim is a
four-legged snake ancestor from Brazil. Though there’s no concrete information
about where this fossil originated, the color and texture of the limestone it
is encased in suggests it’s from the Crato Formation, a fossil deposit which
was laid down some 100 million years ago when the area was a shallow sea.

“The Crato
formation is about 20 million years older than the oldest fossil snake,”
Martill explained. Thus this ten centimeter-long fossil, which Martill and his
colleagues named Tetrapodophis amplectus, may shed light on the earliest
snakes.

“The Martill paper is going to be one of the
most controversial papers around for a long time,” said Lee. “I’ve already had
about 50 emails from colleagues about it, all expressing really different
views.”

“It is a very
unusual specimen,” Lee said, “because if it is a snake, it’s a tremendous
missing link between lizards and snakes.”

But there are
several lineages of lizards with lost or reduced limbs and longer bodies, so
the evidence to place it as a snake ancestor must be more than just that.
Martill notes that the short length of the tail in relation to the body,
structure of the pelvis, impressions of body scales, recurved teeth, high
vertebral count and the shape of the vertebrae all make Tetrapodophis a snake. “This thing is much much more of a snake
than it is of a lizard,” he concluded. But some scientists don’t buy it. “I
think the specimen is important, but I do not know what it is,” University of
Alberta paleontologist Michael Caldwell told Ed Yong from National Geographic. But
Lee is willing to give Martill the benefit of the doubt. “I’m prepared to
provisionally accept that it’s a very unusual small snake,” he said. “But the
specimen is so small and the skull is so badly crushed that I think there is
going to be a lot of debate until all interested researchers are able to look
at it.”

“It does seem to
have some pretty intriguing snake features,” Lee admits. “Snake teeth have a
very distinct curvature to them… and this animal does seem to have that. So
that’s one feature that really makes me think this is probably a snake.” He’s
also impressed by the animal’s spine. “It’s got a very large number of
vertebrae — 160 backbone elements — which is also a very snake-like feature,”
he added. “None of the other features that they list do I find particularly
compelling.”

Hsiang, on the
other hand, is entirely convinced. “Tetrapodophis
does seem to possess many anatomical features that are unique to snakes —
the recurved teeth, intramandibular joint, vertebral characters, et cetera,”
she said. “So, based on Martill et al.’s report of the anatomy, it seems likely
that Tetrapodophis is indeed an early
snake.” She’s especially intrigued by what else is visible in the new fossil:
its last meal. Martill et al. report that inside the snake’s stomach are a
collection of vertebral bones, likely from a small mammal or lizard that it ate
just before it died — the same diet that Hsiang et al. predicted with their
ancestral state analyses. “The new fossil provides empirical confirmation of
some of our results,” she noted. “For instance, the discovery of vertebrate
bones in the stomach contents of Tetrapodophis
aligns with our inference that the earliest snakes likely ate small
vertebrates.”

According to
Martill et al., the short tail and
reduced limbs are evidence that Tetrapodophis
was a burrowing snake. “Although this thing has been found in sediments
that were laid down in water,” Martill says, “the shortened limbs and the
little scoop-like feet that it’s got on its hind limbs look much more like
they’re for burrowing than they are for swimming.”

“Also, they
wouldn’t really function for swimming,” Martill said. “This thing is almost
certainly using lateral undulatory locomotion to burrow through soft sand and
leaf litter.”

“I think that’s
fairly weak evidence,” said Lee. “There’s no living burrowing lizard or snake
with those type of body proportions,” he added. “We can’t really say what it
did at the moment, because there are too many contradictory traits in this
animal.”

Lee similarly
points to the shape and size of the limbs and feet, but says they provide
evidence of an aquatic lifestyle rather than a fossorial one. Species known for
their burrowing habits, like moles, have short, squat, strong limb bones, but Tetrapodophis has “long, delicate
fingers and toes.” There are also questions about the composition of the bones
themselves; bones can vary in the amount of calcium they contain, with more
calcium or “more ossified” bones resisting breakage better than less ossified
ones. Lee notes that the limbs of Tetrapodophis
seem to be “fairly poorly ossified.” “That’s not what you find in burrowers
because you want your hands and feet to be as robust as possible to push
through the soil.” Reduced ossification of limb bones is, however, a trait
shared by other aquatic organisms. Furthermore, in the hind feet, two ankle
bones that are fused in most lizards are separate. The only other group of
lizards where these bones are apart? The aquatic mosasaurs. Rather than seeing
the feet as scoop-like, Lee sees them as “paddle-like.” He also noted that the
bones of the fingers and toes are perfectly aligned in parallel with one
another. “That leads me to think that they were held together in something,
like a flipper or sheath.”

All of that and
the fact that the animal was found in what, at the time, was a shallow sea,
does give credence to the idea that it could be an aquatic snake. “I wouldn’t
come out and say that it’s aquatic, because I don’t think we can say that
either,” Lee said, “but I don’t think that we can conclude that it’s
burrowing.”

The aquatic idea
of snake origins might be the minority view, but there’s enough accumulating
evidence now that it needs to be reexamined rather than dismissed out of hand.”

So how die Brazil’s
Big Discovery end up in Germany?

Though Tetrapodophis is perhaps the most
scientifically-intriguing snake fossil to date, questions about how it arrived
in Germany are already beginning to overshadow its scientific importance. Even
before the paper officially published, rumors swirled about whether the
remarkable specimen was illegally poached from Brazil. When I asked Martill
about the specimen’s discovery, he was disturbingly cavalier about the fossil’s
origins. “More or less, I discovered it,” he said, “I actually found it in a
museum collection.”

“It was one of
those serendipitous things,” he continued.
“I actually worked on fossils from this location in Brazil for many many
years.” But Martill didn’t find Tetrapodophis
on an excursion to the jungle; he found it labeled as an “Unknown Fossil” in
the Bürgermeister-Müller Museum in Solnhofen, Germany on a routine class trip
for his students. It just so happened that when he took his students to see the
museum, on display was an exhibit on Brazilian fossils, which Martill — having
written a book about the Crato formation — was excited to see. “All of a
sudden, my jaw just dropped to the floor,” he recounts. “This looks like a
snake!”

When pressed, he
admitted that there was no information about the fossil’s origins — when it was
found, who pulled it from the earth, and how or why it made its way across the
ocean to a small museum in Germany. He was blunter when he spoke to Herton Escobar
(quoted by Herton Escobar for Science). Martill told him that
questions about legality are ‘irrelevant to the fossil’s scientific
significance’ and said: “Personally I don’t care a damn how the fossil came
from Brazil or when.”

As Shaena
Montanari explains for Forbes, given the laws in Brazil
since 1942, it’s likely that Tetrapodophis
found its way to Europe illegally. Brazilian officials have gone as far as to
say they’re certain the specimen illegally left the country. Many scientists
are expressing their outrage that a prestigious journal like Science
would even publish a paper based upon what is likely a black market specimen.

Thus, the specimen
is controversial by its very nature but the issue of it being in Germany
illegally also raises questions about the fossil trade.

References

Martill, Tischlinger & Longrich. (2015). A
four-legged snake from the Early Cretaceous of Gondwana.Science.
doi: 10.1126/science.aaa9208

Hsiang et al. (2015). The origin of snakes:
revealing the ecology, behavior, and evolutionary history of early snakes using
genomics, phenomics, and the fossil record.BMC
evolutionary biology, 15(1), 87. doi:10.1186/s12862-015-0358-5

Sunday, July 5, 2015

Fragmented tropical forest landscapes are becoming
more abundant, and loss of species following fragmentation are often
predictable. Larger animals, tend to disappear first from fragments due to the
bushmeat trade. However, another vulnerable
group includes understory, insectivorous birds, and ant-following birds. Nest
predation is one mechanism that may limit bird populations and has long been
suspected as a factor threatening bird populations in temperate and tropical forest fragments. A potential influence on nest predation that
remains understudied in the tropics is density dependence. Dense territories
can increase predators’ ability to find the closely-spaced nests. Yet bird
density and nest predation are not always positively correlated, and multiple
life-history traits and contexts are relevant.

A climate-induced change of male dragons
into females occurring in the wild has been confirmed for the first time,
according to University of Canberra research recently published on the cover of
international journal Nature.

The researchers, who have long studied
Australia's bearded dragon lizards, have been able to show that a reptile's sex
determination process can switch rapidly from one determined by chromosomes to
one determined by temperature.

Lead author Dr. Clare Holleley, a
postdoctoral research fellow at the University of Canberra's Institute for
Applied Ecology, explained: "We had previously been able to demonstrate in
the lab that when exposed to extreme temperatures, genetically male dragons
turned into females."

"Now we have shown that these sex
reversed individuals are fertile and that this is a natural occurring
phenomenon."

Using field data from 131 adult lizards
and controlled breeding experiments, Dr Holleley and colleagues conducted
molecular analyses which showed that some warmer lizards had male chromosomes
but were actually female.

"By breeding the sex reversed
females with normal males, we could establish new breeding lines in which
temperature alone determined sex. In doing so, we discovered that these lizards
could trigger a rapid transition from a genetically-dependent system to a
temperature-dependent system," she said.

"We also found that sex-reversed
mothers -- females who are genetic males -- laid more eggs than normal
mothers," Dr Holleley said. "So in a way, one could actually argue
that dad lizards make better mums."

University of Canberra Distinguished
Professor Arthur Georges, senior author of the paper, also highlighted the
importance that these discoveries have in the broader context of sex
determination evolution.

"The mechanisms that determine sex
have a profound impact on the evolution and persistence of all sexually
reproducing species," Professor Georges said.

"The more we learn about them, the
better-equipped we'll be to predict evolutionary responses to climate change
and the impact this can have on biodiversity globally."

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